INTRODUCTION
Centers of endemism and geographically clustered hybrid zones are
hypothesized to be the legacy of species persistence through the
Pleistocene in multiple ice-free glacial refugia followed by population
expansion and contact (Hultén 1937; Heusser 1989; Heaton & Grady 2003;
Swenson & Howard 2005). Isostatic adjustment and lower sea-levels (Mann
1986) are credited with exposing areas of the continental shelf along
North America’s North Pacific Coast (NPC) and providing terrestrial
sanctuary for insular and coastal species displaced by the expanding
Cordilleran and Laurentide ice sheets (Heaton et al. 1996; Hewitt
2000; Lacourse et al. 2003; Mathewes & Clague 2017). Multiple
refugia are hypothesized within southeast Alaska’s contemporary
Alexander Archipelago (e.g., Baranof, Chichagof, Dall, Heceta, and
Prince of Wales islands; Foster 1965; Fedorov & Stenseth 2002; Carrara
et al. 2003, 2007; Ager 2019) and British Columbia’s Haida Gwaii
Archipelago and surrounding areas (Heusser 1989; Mathewes & Clague
2017). Ice-free coastal refugia may have also played an integral role in
human colonization of the Americas by opening a maritime migration
corridor. New evidence shows the Pacific Northwest was inhabited by
humans as early as > 15-16 thousand years ago (kya; Devièseet al. 2018; Davis et al. 2019) and the Alexander
Archipelago at least > 10 kya, but likely more than 13 kya
(Dixon et al. 2014; Carlson & Baichtal 2015; Lesnek et al. 2018;
Mackie et al. 2018; McLaren et al. 2018), potentially
predating the opening of an ice-free migration corridor through central
Alberta, Canada (<=14.8 kya; Margold et al. 2019). An
incomplete fossil record, however, creates uncertainty over which
species persisted in hypothesized refugia, obscuring interpretation of
their duration and paleoenvironments. Unlike humans with access to
rudimentary sea-faring technologies (Erlandson et al. 2007),
other coastal refugial mammals would have been essentially isolated from
mainland populations, leading to a cessation in gene flow and divergence
over time (Hewitt 2000). As such, the genomes of refugial descendants
can provide clues to whether populations or species diverged in refugial
isolation. Predicted variation includes high genetic differentiation
from other refugial populations and the abundance of endemic or
ancestral alleles, low genetic diversity as a consequences of small
population sizes and genetic drift, and less spatial structure relative
to recently colonized populations (Hewitt 2000).
In contrast to glacial isolation, post-glacial population expansion from
multiple refugia can lead to secondary contact and the formation of
hybrid zones between previously isolated taxa (Hewitt 2000; Swenson &
Howard 2005). The rapid climatic oscillations of the Pleistocene
(Williams 1998) led to recurrent opportunities for contact and gene flow
between incompletely diverged taxa (Hewitt 2000, 2003). The consequences
of genetic exchange are complex and range from homogenization to hybrid
speciation (Arnold 1997; Harrison & Harrison 1993; Genovart 2009;
Abbott et al. 2016), depending on the level of differentiation,
but they can now be examined in detail using whole-genome sequences
(Twyford & Ennos 2012).
North American martens are relatively small meso-carnivores,
hypothesized to have diverged in at least two independent glacial
refugia south of the Laurentide ice sheet (Stone et al. 2002):
one refugium east of the Rocky Mountains or Mississippi River drainage
giving rise to American pine martens (Martes americana , Turton
1806) and another to the west, presumably the cradle for Pacific martens
(Martes caurina , Merriam 1890). However, the disjunct
contemporary range of Pacific martens and occurrence of two natural
hybrid zones between these species\(\ \) one occurring on near-coastal
islands (Kuiu and Kupreanof, AK) along the NPC and another in the
northern Rocky Mountains (Fig. 1)\(\ \) suggest Pacific martens may have
a deeper evolutionary history along the NPC than previously thought
(Pauli et al. 2015). The widespread coast-to-coast boreal
distribution of M. americana directly contrasts with the
fragmented distribution of M. caurina, found along the Pacific
coast (CA, OR, WA), mountaintops of the American Southwest (NM, CO, UT)
and northward into Montana and Idaho, and four islands within the
putative refugial archipelagos of the NPC: Graham, Moresby, Kuiu, and
Admiralty islands.
In addition to two natural hybrid zones, a series of intentional
wildlife translocations in the mid-1900s introduced M. americanato multiple NPC islands without prior knowledge of the native marten
species in the region (Powell et al. 2012). While these
introductions may complicate the interpretation of genomic signals from
this region, they also provide a framework for interpreting the
consequence of natural versus anthropogenically-mediated gene flow on
the evolution and persistence of species. Accidental introductions
(Fenichel et al. 2008; Weber et al. 2017) or intentional,
motivated by economics (McNeely 2001; Fenichel et al. 2008;
Powell et al. 2012), public safety (Massei et al. 2010) or
conservation (Powell et al. 2012), are increasingly common and
can result in unanticipated consequences, including hybridization with
native species (Todesco et al. 2016) and exchange of parasites
(Prenter et al. 2004) with unknown evolutionary outcomes. Genetic
management techniques, including genetic rescue (Whiteley et al.2015) or gene tweaking (Thomas et al. 2013), are increasingly
proposed as viable mechanisms to boost diversity in small inbred
populations. Application of these techniques can be informed through
investigations of existing hybrid zones and historical wildlife
translocations which can cumulatively inform a predictive framework for
anticipating the evolutionary consequences of genetic exchange. In
martens, hybridization may disproportionately impact Pacific martens
through genetic dilution from outbreeding (Colella et al. 2018a).
Low genetic variation in certain insular populations of M.
caurina (Stone et al. 2002; Small et al. 2003) has led to
further concerns over their persistence, which may be exacerbated by
ongoing harvest of forests and extraction of minerals on those islands
(Durbin 1999; USDA 2018).
We use whole-genome resequencing data to refine our understanding of the
biogeographic history of NPC martens and place these results within the
context of the Coastal Refugium Hypothesis (CRH; Heusser 1989; Scudder
& Gessler 1989; Heaton et al. 1996; Demboski et al. 1999;
Sawyer et al. 2019). With increased molecular resolution, we
explore the evolutionary consequences of introgression in New WorldMartes to further inform natural resource management initiatives.
We examine the distribution of geographic variation and estimate the
timing and directionality of introgression to assess the role of natural
hybridization, historic wildlife translocations, natural colonization
events, and glacial cycling in shaping the evolution of New World
martens.